REVIEW published: 06 August 2015 doi: 10.3389/fpls.2015.00573 Secondary metabolites in fungus-plant interactions Tünde Pusztahelyi 1*, Imre J. Holb 2, 3 and István Pócsi 4 1 Central Laboratory, Faculty of Agricultural and Food Sciences and Environmental Management, University of Debrecen, Debrecen, Hungary, 2 Faculty of Agricultural and Food Sciences and Environmental Management, Institute of Horticulture, University of Debrecen, Debrecen, Hungary, 3 Department of Plant Pathology, Centre for Agricultural Research, Plant Protection Institute, Hungarian Academy of Sciences, Debrecen, Hungary, 4 Department of Biotechnology and Microbiology, Faculty of Science and Technology, University of Debrecen, Debrecen, Hungary Fungi and plants are rich sources of thousands of secondary metabolites. The genetically coded possibilities for secondary metabolite production, the stimuli of the production, and the special phytotoxins basically determine the microscopic fungi-host plant interactions and the pathogenic lifestyle of fungi. The review introduces plant secondary metabolites usually with antifungal effect as well as the importance of signaling molecules in induced systemic resistance and systemic acquired resistance processes. The review also concerns the mimicking of plant effector molecules like auxins, gibberellins and Edited by: abscisic acid by fungal secondary metabolites that modulate plant growth or even can Essaid Ait Barka, subvert the plant defense responses such as programmed cell death to gain nutrients for University of Reims Champagne-Ardenne, France fungal growth and colonization. It also looks through the special secondary metabolite Reviewed by: production and host selective toxins of some significant fungal pathogens and the plant Michael Wink, response in form of phytoalexin production. New results coming from genome and Heidelberg University, Germany Xiquan Gao, transcriptional analyses in context of selected fungal pathogens and their hosts are also Nanjing Agricultural University, China discussed. *Correspondence: Keywords: host-pathogen interaction, phytotoxin, phytoalexin, secondary metabolite, mycotoxin Tünde Pusztahelyi, Central Laboratory, Faculty of Agricultural and Food Sciences and Environmental Management, Introduction University of Debrecen, Böszörményi út 138, H-4032 Debrecen, Hungary Phytopathogenic fungi that are basically classified as necrotrophs, hemibiotrophs and biotrophs [email protected] constitute one of the main infectious agents in plants, causing alterations during developmental stages including post-harvest, gaining nutrients from the plants they invade and, therefore, Specialty section: resulting in huge economic damage. Plants and fungi are rich sources of thousands of secondary This article was submitted to metabolites (SMs), which consist of low-molecular weight compounds (the number of the Plant Biotic Interactions, described compounds exceeds 100,000) that are usually regarded as not essential for life while a section of the journal their role are quite versatile (Perez-Nadales et al., 2014; Scharf et al., 2014). Here, our primary Frontiers in Plant Science aims were to overview the fungal-plant interactions and summarize special SM productions Received: 29 March 2015 (e.g., phytotoxins and phytoalexins) in context of these interactions. Furthermore, the review Accepted: 13 July 2015 also considers data from new fungal genome and transcriptome analyses. These data have Published: 06 August 2015 Citation: Abbreviations: ABA, abscisic acid; AF, aflatoxin; AF B1, aflatoxin B1; AF B2, aflatoxin B2; AF G1, aflatoxin G1; DMATS, Pusztahelyi T, Holb IJ and Pócsi I dimethylallyl tryptophan synthetase; DON, deoxynivalenol; ET, ethylene; FB1, fumonisin B1; FB2, fumonisin B2; JA, jasmonic (2015) Secondary metabolites in acid; IAA, indole-3-acetic acid; ISR, induced systemic resistance; HST, host-selective toxin; NHST, non host-selective toxin; fungus-plant interactions. NRPS, non-ribosomal protein synthase; PCD, programmed cell death; PKS, polyketide synthase; PR, pathogenesis-related; Front. Plant Sci. 6:573. ROS, reactive oxygen species; SA, salicylic acid; SAR, systemic acquired resistance; SM, secondary metabolite; TS, tryptophan doi: 10.3389/fpls.2015.00573 synthetase; ZEA, zearalenone. Frontiers in Plant Science | www.frontiersin.org 1 August 2015 | Volume 6 | Article 573 Pusztahelyi et al. Fungal-plant interaction hypothesized the biosynthesis of a much wider spectrum of SMs composed of moieties from different classes are common, as in than we have actually isolated and characterized, and which the meroterpenoids, which are fusions between terpenes and could have strong effect on crop quality. In addition, these data polyketides. Analysis of available fungal genomes revealed that proposed more possible physiological activities for the SMs than ascomycetes have more genes of secondary metabolism than we thought before. basidiomycetes, archeo-ascomycetes, and chytridiomycetes, whereas hemi-ascomycetes and zygomycetes have none Phytopathogenic Fungi (Collemare et al., 2008). Ascomycete genomes code for on average 16 polyketide synthases (PKS), 10 non-ribosomal Lifestyle of Phytopathogenic Fungi protein synthases (NRPS), two tryptophan synthetases (TS), While the initial phases of pathogenesis do not differ and two dimethylallyl tryptophan synthetases (DMATS) with fundamentally between necrotrophs, hemibiotrophs and obligate crucial importance in SM synthesis. These types of SM genes biotrophic fungi, different strategies are used to acquire nutrients. encode signature enzymes that can be enriched in secondary Necrotrophic fungi have broader host ranges than biotrophs metabolism gene clusters and responsible for main synthesis and often enlist cell-wall-degrading enzymes and toxins, which steps of metabolites. PKS–NRPSs have been identified only can be small peptides or SMs (Howlett, 2006). In contrast to in ascomycetes, with an average of three genes per species. necrotrophic and hemibiotrophic fungal pathogens, obligate Neurospora crassa as well as human pathogens Coccidioides spp. biotrophs are entirely dependent on living plant tissue and and Histoplasma capsulatum have a lower number of PKSs (1–9 characterized by a number of sophisticated infection structures genes), NRPS (3–6 genes) and PKS-NRPSs (0–2 genes) than including appressoria, penetration hyphae and infection hyphae other ascomycetes. High number of fungal species have more allowing the invader to suppress plant defense responses and to than 40 genes encoding PKS, NRPS, hybrids, TS, and DMATS in gain excess to host nutrients (reviewed by Mendgen and Hahn, their genome, including M. grisea (45 genes) (Collemare et al., 2002; Schulze-Lefert and Panstruga, 2003). Biotrophs establish 2008) (Table 1). Synthesis of siderophores, a class of SMs for haustoria for nutrient uptake (Panstruga, 2003), suppress iron uptake also involves a NRPS that is also very important for induction of host defense and reprogram metabolism (Biemelt the virulence of several fungi (e.g., Cochliobolus heterostrophus, and Sonnewald, 2006). Biotrophic fungi and their metabolism C. miyabeanus, F. graminearum, and A. brassicicola)(Oide et al., has been studied on nonobligate biotrophs, such as Cladosporium 2006). fulvum (Thomma et al., 2005), Magnaporthe grisea (Talbot, 2003) Whole-genomic analysis have identified 12–15 PKS genes and Mycosphaerella graminicola (Palmer and Skinner, 2002; in F. graminearum (Kroken et al., 2003; Gaffoor and Trail, Deller et al., 2011). Much less is known about the obligate 2006; Gao et al., 2014; Sieber et al., 2014), where six have been biotrophs, such as powdery mildews or rust fungi. However, it linked to metabolites. The remaining PKSs have no assigned appears that biotrophy is associated with a convergent loss of products yet even though they were expressed under tested secondary metabolic enzymes and reduction in genes encoding conditions. In F. graminearum, the genes with known functions specific transporters of toxin secretion and extrusion of host (13 SM genes) cover only a minor fraction of the 51 predicted defense compounds usual in necrotrophic fungi. Nevertheless, SM genes: 15 PKSs, 19 NPSs and 17 TSs were identified the infection strategy of necrotrophic fungi is less complex (Sieber et al., 2014). Besides the classical SM genes (TS, NPS, than that of obligate biotrophs. Appressoria formed by typical and PKS) the 114 predicted genes encoding cytochrome P450 necrotrophs such as Cercospora, Ramularia, Rhynchosporium, enzymes are also suitable candidates for searching SM gene Alternaria, Fusarium, Botrytis, Helminthosporium, Sclerotinia, clusters. Cytochrome P450s play an essential role in many known or Verticillium species, are inconspicuous, and infection biosynthetic pathways of fungal compounds, for instance in the hyphae formed within the host are quite uniform (reviewed biosynthesis of trichothecene mycotoxins (Tokai et al., 2007) and by Horbach et al., 2011). Condon et al. (2013) suggested that, gibberellins (Hedden et al., 2001)(Figure 1). while necrotrophs and hemibiotrophs employ fundamentally In the Macrophomina phaseolina anamorphic fungus from contrasting mechanisms of promoting disease, the tools they the ascomycete family Botryosphaeriaceae, Islam et al. (2012) utilize e.g., host-selective toxins (HST) and protein effectors identified 75 putative SM genes compared with 32 in M. grisea, basically overlap. 37 in B. cinerea, 29 in S. sclerotiorum, and 37 in F. graminearum. It cannot be forgot that there are numerous